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Concerns over bees, especially the European honey bee (Apis mellifera)
have rarely been higher. Although there are few hard data there is a general
consensus that both solitary and social bee populations are declining
and that recently the still-mysterious colony collapse disorder (CCD)
has dramatically worsened this situation. No definitive cause for CCD
has yet been established but there is widespread agreement that CCD is
caused by more than one factor (Calderone, 2008 ; Oldroyd, 2007).

One of the speculated contributors to this decline is transgenic crops
and specifically those containing Bt proteins since these are
insect-active toxins to which bees are exposed through various routes.
In particular, bee larvae are exposed since they consume large quantities of pollen which they sometimes source from maize plants
(Sabugosa-Madeira et al. 2007). Up to now however there has been no
specific evidence that any Bt toxin has negative effects on bees, but
equally such studies have been rare. Particularly lacking are studies
on sub-lethal effects of Bt toxins on bees.

In the view of many, there is clear evidence from laboratory settings
that Bt toxins can affect non-target organisms. Usually, but not
always, affected organisms are closely related to intended targets
(reviewed in Lovei and Arpaia 2005 and Hilbeck and Schmidt 2006).
Typically, exposure is through the consumption of plant parts such as
pollen or plant debris or through Bt ingested by their predatory food
choices. Nevertheless, due to significant data gaps, the real-world
consequences of Bt transgenics remains unclear.

Thus the lepidopteran-active Cry1Ab is, not unexpectedly, toxic to some
butterflies (e.g. Losey et al 1999 and Lang and Vojtech 2006) while
more distantly-related organisms affected by Cry1Ab are ladybird
larvae, caddisflies and Daphnia Magna (Rosi-Marshall et al 2007; Bøhn
et al 2008; Schmidt et al 2008). Other variants of Bt, such as Cry3Bb,
are considered coleopteran-active but have been the subject of less
research. Nevertheless, these may also affect non-target coleopterans
such as ladybird larvae as well as more distantly related organisms
such as lacewings (Hilbeck and Schmidt 2006; Schmidt et al 2008).

A recent paper adds to the non-target story by demonstrating that honey
bees fed on the active form of purified Cry1Ab protein can be affected
in the learning responses necessary to associate nectar sources with
odourants (Ramirez-Romero et al 2008). This learning response is
important in bee foraging behaviour and it has attracted the attention
of CCD researchers since it is known to be inhibited by the insecticide
imidacloprid (e.g. Decourtye et al 2004). In this latest study bees
consuming artificial nectar containing 5000ppb of Cry1Ab continued to
respond positively to a learned odour even in the absence of a food
reward, while normal bee behaviour is to become discouraged and seek
more abundant food sources.

Left unstudied by the authors however was the likely mode of action of
this behavioural effect. This is of considerable interest since the
principal means of Bt lethality, which is thought to be a
receptor-mediated effect on gut integrity, fails to explain the
observed behavioural modification. The new finding is therefore
particularly interesting since it lends weight to a previous suggestion
that Bt toxins may have other, non-lethal effects which become apparent
only when the normal (i.e. lethal) effect is absent (Hilbeck and
Schmidt 2006; Schmidt et al. 2008). If there were to be multiple modes
of Bt action then many more non-target organisms would likely be at
risk from Bt transgenics.

The authors propose that bees are unlikely to be exposed to the
quantity of Cry1Ab that led to the defects in behaviour they observed.
However, this conclusion seems premature since Bt concentrations in
plants are highly variable (Lorch and Then 2007). It is also probable
that in real situations bees may be exposed earlier in their development
and over longer periods. Bt Researcher Angelika Hilbeck believes that
experiments simulating real-world bee experiences are still lacking.
“What really needs to be looked at are combinations of both the Bt
toxin AND imidacloprid and not Bt toxin OR imidacloprid, and in a form
that simulates the exposure routes in the field”.

References

Bøhn T., Primicerio R., Hessen D.O., Traavik T. (2008) Reduced Fitness
of Daphnia magna Fed a Bt-Transgenic Maize Variety. Arch. Environ.
Contam. Toxicol. 55:584-92

Decourtye A.; Armengaud C., Renouc M.; Devillers J.; Cluzeau S.;
Gauthier M. and Pham-Delègue M-H. (2004) Imidacloprid impairs memory
and brain metabolism in the honeybee (Apis mellifera L.). Pesticide
Biochemistry and Physiology 78: 83-92

Hilbeck A. and Schmidt J.E.U. (2006) Another View on Bt Proteins – How
Specific are They and What Else Might They Do? Biopestic. Int. 2: 1-50

Lang A. and Vojtech E. (2006) The effects of pollen consumption of
transgenic Bt maize on the common swallowtail, Papilio machaon L.
(Lepidoptera, Papilioni). Basic and Applied Ecology 7: 296-306

Lövei G.L. and Arpaia S. (2005) The impact of transgenic plants on
natural enemies: a critical review of laboratory studies. Entomologia
Experimentalis et Applicata 114: 1-14

Lorch A. and Then C. (2007) How much Bt toxin do MON810 plants actually Produce? www.greenpeace.de/fileadmin/gpd/user_upload/themen/gentechnik/greenpeace_bt_maize_engl.pdf

Losey J.E. Rayor L.S.; and Carter M.E. (1999)Transgenic pollen harms monarch larvae Nature 399: 214

Oldroyd B. (2007) What’s Killing American Honey Bees? PLoS Biol 5(6)

Ramirez-Romero R.; Desneux N.; Decourtye A.; Chaffiol A.; Pham-Delègue
M.H. (2008)Does Cry1Ab protein affect learning performances of the
honey bee Apis mellifera L. (Hymenoptera, Apidae)? Ecotoxicol Environ
Saf. 70:327-33

Rosi-Marshall, E.J.; J. L. Tank; T. V. Royer; M. R. Whiles; M.
Evans-White; C. Chambers; N. A. Griffiths; J. Pokelsek and M. L.
Stephen (2007) Toxins in transgenic crop byproducts may affect
headwater stream ecosystems. Proc Natl Acad Sci USA 104: 16204–16208

Sabugosa-Madeira B.; Abreu I.; Ribeiro H. and Cunha M. (2007) Bt
transgenic maize pollen and the silent poisoning of the hive Journal of
Apicultural Research 46: 57-58

Schmidt J.E.; Braun C.U.; Whitehouse L.P.; Hilbeck A. Effects of
Activated Bt Transgene Products (Cry1Ab, Cry3Bb) on Immature Stages of
the Ladybird Adalia bipunctata in Laboratory Ecotoxicity Testing. Arch
Environ Contam Toxicol. 2008 Aug 20